Endosymbiotic bioenergetic synergy behind climate-mediated species boundaries of rainforest warblers

Dahong Chen, Silu Wang

The molecular cooperation among organelles facilitates adaptation during eukaryotic evolution, but the role of endosymbiotic synergy in the organismal climate adaptation remains unclear. Here we unveil the Endosymbiotic Bioenergetic Synergy Model, which characterizes the role of emergent molecular activities among organelles underlying energy metabolism in climate adaptation of eukaryotes. The hybridizing wood warblers experiencing dramatic climate changes in the Pacific Northwest provide natural recombination experiments to understand the molecular genomic responses to climate change. Integrating life history morphometrics, cell-type-specific multiomics, biochemical analyses and confocal imaging, we discovered the endosymbiotic bioenergetic synergy among nucleus, mitochondria, and ribosome at the molecular foundation of climate adaptation. We further elucidated adaptive inertia in the forms of oxidative stress and OXPHOS inefficiency that can be partially alleviated by the introgression of warm-adapted endosymbiotic genetic variants across the species boundaries. This synergistic insight in endosymbiotic bioenergetics has broad implication for understanding eukaryotic cells over space and time.